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1 Tropical Biomedicine 31(1): (2014) Gastrointestinal parasites of birds in zoological gardens in south-west Nigeria Otegbade, A.C. and Morenikeji, O.A. * Department of Zoology, University of Ibadan, Ibadan, Nigeria * Corresponding author Received 27 July 2013; received in revised form 16 September 2013; accepted 21 September 2013 Abstract. Infections with gastrointestinal parasites are a major health issue in captive birds. However, prevalence data of gastrointestinal parasites of birds in zoological gardens in Nigeria are scarce. This study was carried out to establish the gastrointestinal parasite profile of birds kept in zoological gardens in the University of Ibadan, Obafemi Awolowo University, University of Ilorin, University of Lagos and Federal University of Agriculture Abeokuta, all in south-west Nigeria. A total of 178 fecal samples from 83 birds (14 species in eight orders) were examined using three techniques; Feacal sedimentation using ethyl acetate, McMaster Egg Counting Technique and Petri Dish- Filter Paper Slant culture technique (modified Harada- Mori Technique). A total of 39(21.9%) of the 178 samples were infected. The highest prevalence (100%) of infection was recorded in Unilag zoo and a total of five species of parasites including two protozoans (coccidian and Balantidium spp.); and three nematodes Capillaria spp., Ascaris spp. and Strongyloides spp.) were recorded with Capillaria spp. (14.1%) as the most prevalent gastrointestinal parasite. Mixed infections were found in 18(10.1%) samples. Strongyloides larvae were observed in 6(3.4%) samples. All Anseriformes were infected but the Struthioniformes had the highest infection rate. The geometric mean intensity of eggs ranged from ± to ± epg and oocyst counts ranged from ± to ± opg. Balantidium cyst count was ± Count of oocyst of coccidian species was significantly higher in all the zoos. The feacal culture yielded Strongyloides species. Regular deworming and hygienic measures are necessary to prevent gastrointestinal infections in captive birds. So also, improved funding and management are necessary to ensure sustainability of Nigerian zoological gardens. INTRODUCTION Zoological gardens exhibit wild animals for aesthetic, educational and conservation purposes. However, parasitic diseases constitute one of the major problems causing mortality in these animals while in captivity (Rao & Acharjyo, 1984; Varadharajan & Kandasamy, 2000). The effects range from sub-clinical to death. In 2003, Nigeria was said to be the seasonal, breeding or year round home of 906 species of birds (FEPA, 2003), three of the twelve species that are indigenous to Nigeria are threatened. These are the Anambra waxbill (Estrilda popliopareia), Ibadan malimbe (Malimbus ibadanensis) and Jos plateau indigo bird (Vidua maryae) (Aminu- Kano, 2001). Some of these birds are kept in Nigerian zoos. Parasites usually cause little or no distress to healthy individuals in the wild; however parasitic infections are among the most common sanitary problems affecting captive birds, especially in highdensity populations (Barnes, 1986). Despite the fact that there is a large body of literature on avian medicine including parasitic diseases (Altman et al., 1997; Rupley, 1997; Olsen & Orosz, 2000), little has been documented about the epidemiology of gastrointestinal parasites in zoo birds. Some published studies included case reports (Kwon et al., 2005; Luppi et al., 2007; Ferrell et al., 2009) or surveys on a single parasitic 54

2 agent (Rohela et al., 2005; Schoener, 2010; Wang et al., 2011), while others examined intestinal parasites in a limited range of zoo species (Sotirakis et al., 2001; Hollamby et al., 2003; Fallacara et al., 2004; Yusufu et al., 2004; Pheng et al., 2005; Ibrahim et al., 2006; Perez-Cordon et al., 2008; Khan et al., 2010; Mshelia et al., 2010). Only a few coprological surveys were carried out in a wide range of avian species displayed in zoo settings (Patel et al., 2000; Parsani et al., 2003; Perez- Cordon et al., 2009; Ajibade et al., 2010; Akinboye et al., 2010; Gurler et al., 2010; Opara et al., 2010; Papini et al., 2012 ). There is no doubt that a regular program of surveillance and measures of gastrointestinal parasites with correct diagnosis, effective treatment and proper prophylaxis would assist in maintaining good health of zoo birds. By trying to establish a profile of gastro-intestinal parasites in the zoo birds, valuable information will be obtained for the development of public health and preventive medicine. This study was therefore carried out to identify and determine the prevalence and intensity of gastrointestinal parasites of kept birds in five zoological gardens in South West Nigeria. MATERIALS AND METHODS Study Area The study was conducted from March to May 2012 in five zoological gardens in South-West Nigeria; University of Ibadan (U.I), Obafemi Awolowo University (OAU), University of Ilorin (Unilorin), University of Lagos (Unilag) and Federal University of Agriculture Abeokuta (FUNAAB) Zoological Gardens. There are a variety of animal species in these zoos, including non human primates, carnivores, herbivores, birds, and reptiles. The bird collections are composed of several species housed separately in cages or aviary depending on their size. Some birds are housed in uncemented enclosures while some in cemented enclosures. In the Unilorin zoo, most of the species are free ranging during the day and housed at night. Cages are cleaned daily in all of the zoos. The climate in south west Nigeria is characterized by both wet and dry seasons and relatively high humidity. The mean annual rainfall is about 1200mm (Olaniran, 2002). Study Animals A total of 178 fecal samples from 14 bird species in 8 orders were examined in the five zoological gardens (Table 1). Sample Collection Freshly passed feacal samples of birds were collected early in the morning before routine cleaning of all cages in each zoo. All samples were picked from the ground by utilizing a new sterile polystyrene spatula for each bird species to avoid cross contamination. In cases of small and medium sized zoo birds, multiple faecal droppings were pooled from all birds of the same species to collect an adequate amount of faeces for parasitological examination. Feacal samples of ostriches were collected from each bird. Samples were collected in plastic vials, which were clearly marked with the time, date of collection and species or subspecies of the bird. All samples were transported to the laboratory, and examined within 48 hrs. Collected samples were examined macroscopically for consistency, presence of blood, mucus, and tapeworm proglottids. Parasitological Techniques All the samples were examined for parasite eggs and larvae using standard methods. Qualitative egg identification was done by fecal sedimentation technique using ethyl acetate, McMaster Egg Counting Technique (MAFF, 1977) for egg, oocyst and cyst count and larva culture was done using the Petri Dish- Filter Paper Slant culture technique (modified Harada- Mori Technique) as described by Garcia (2001). Some quantity of each faecal sample was cultured for 10 days (Soulsby, 1982), to harvest and identify helminth larvae. Identification of helminth ova, oocyst and infective larvae was done by using the keys by Soulsby (1982) and Sloss et al. (1994). 55

6 during the day and housed at night. Most of the birds were fed with grains. Ostriches were fed with grass and vegetable collected from or around the zoo grounds while the accipitriform birds were fed with fish. Furthermore, all the parasites found in this study were transmitted faecal-orally through contaminated soil, food, and water. As a result, these may play a key role as sources of parasite infection to birds under captivity conditions. In the five zoos, gastrointestinal helminthes were more prevalent than protozoans and this comprised mainly of nematodes. This finding agrees with the reports of Rossanigo & Gruner (1995) that nematodes were responsible for most of the helminth diseases of veterinary importance, because they don t need intermediate hosts. Generally, the most common infection was of Capillaria spp. which was followed by Ascaris spp. and coccidian species, while the lowest was Balantidium spp. which occurred in two samples of same bird species. More than 10% of the examined faecal samples of birds had mixed infections. There was mixed infection of Capillaria and Coccidian spp., Capillaria and Ascaris spp., Capilaria and Strongyloides spp. and Ascaris and coccidian spp. The most frequently encountered gastrointestinal parasite, Capillaria spp. are small roundworms that infect the small intestine and infection is usually asymptomatic, but birds with heavy parasite burden may show clinical signs of anorexia, diarrhoea, emaciation, reduced water intake, ruffled feathers, and weakness (Yabsley, 2009). None of the infected birds with Capillaria spp. in this study showed clinical signs. Ascaris spp. are the largest nematodes of birds and generally inhabit the small intestine. They are usually not pathogenic in slight infection. However, they can produce overt clinical disease and even death if their number is sufficiently high enough to cause anaemia, severe inflammatory response, and starvation (Fagerholm & Overstreet, 2009; Fedynich & Thomas, 2009). None of the infected birds with Ascaris spp. showed clinical signs in this study. Intestinal coccidiosis occurring in birds includes species of the genera Eimeria, Isospora, Tyzzeria, and Wenyonella (Friend & Franson, 1999). They can be distinguished by the characteristic morphology of their sporulated oocysts that differ mainly in number of sporocysts and sporozoites (Yabsley, 2009). In this study, unsporulated oocysts were found in faecal samples from five mallard ducks, two water birds, and two geese belonging to the orders Anseriformes, two parrots of the order Pscittaciformes and three ostriches of the order Struthioniformes. Previous studies have shown that Eimeria and Isospora infections can occur in Psittaciformes, Struthioniformes and Anseriformes (Friend & Franson, 1999; Patel et al., 2000; Ibrahim et al., 2006; Yabsley, 2009). Neither Tyzzeria nor Wenyonella is known to occur in avian species belonging to these orders (Friend & Franson, 1999). Therefore, the genera Eimeria and Isopora were thought to be the most likely cause of coccidian infection in this survey. Clinical signs of intestinal coccidiosis include watery, mucoid, or bloody diarrhoea, decreased egg production, emaciation, lack of appetite, lethargy, lack of coordination, ruffled feathers, and weight loss (Yabsley, 2009). None of the infected birds with intestinal coccidiosis showed clinical signs in this study. Generally egg counts were low compared to oocyst count. Eggs and oocyst counts were high in Unaab zoo than in other zoos. The intensity of coccidian species is higher than other parasite species even though its prevalence in the birds is moderate. All parasites found in this study were reported by Mbaya et al. (2006) and Ibrahim et al. (2006) in earlier studies, except Strongyloides spp. larvae. The presence of high parasite prevalence in OAU and Unilorin zoos, despite the use of parasiticide, demonstrated that the anthelminthic program in these zoological gardens needs to be re-evaluated by means of therapeutical trials to assess drug efficacy and possible nematodicide resistance of these parasites. 59

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